Characterization of <i>Anopheles gambiae</i> D7 salivary proteins as markers of human–mosquito bite contact

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Abstract

Background

Malaria is transmitted when infected Anopheles mosquitoes take a blood meal. During this process, the mosquitoes inject a cocktail of bioactive proteins that elicit antibody responses in humans and could be used as biomarkers of exposure to mosquito bites. This study evaluated the utility of IgG responses to members of the Anopheles gambiae D7 protein family as serological markers of human–vector contact.

Methods

The D7L2, D7r1, D7r2, D7r3, D7r4 and SG6 salivary proteins from An. gambiae were expressed as recombinant antigens in Escherichia coli. Antibody responses to the salivary proteins were compared in Europeans with no prior exposure to malaria and lifelong residents of Junju in Kenya and Kitgum in Uganda where the intensity of malaria transmission is moderate and high, respectively. In addition, to evaluate the feasibility of using anti-D7 IgG responses as a tool to evaluate the impact of vector control interventions, we compared responses between individuals using insecticide-treated bednets to those who did not in Junju, Kenya where bednet data were available.

Results

We show that both the long and short forms of the D7 salivary gland antigens elicit a strong antibody response in humans. IgG responses against the D7 antigens reflected the transmission intensities of the three study areas, with the highest to lowest responses observed in Kitgum (northern Uganda), Junju (Kenya) and malaria-naïve Europeans, respectively. Specifically, the long form D7L2 induced an IgG antibody response that increased with age and that was lower in individuals who slept under a bednet, indicating its potential as a serological tool for estimating human–vector contact and monitoring the effectiveness of vector control interventions.

Conclusions

This study reveals that D7L2 salivary antigen has great potential as a biomarker of exposure to mosquito bites and as a tool for assessing the efficacy of vector control strategies such as bednet use.

Graphical abstract

Supplementary Information

The online version contains supplementary material available at 10.1186/s13071-021-05130-5.

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Most cited references 30

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Variation in malaria transmission intensity in seven sites throughout Uganda.

Patricia Roelants, Umberto D’Alessandro, A Correwyn … (2006)

Knowledge of the baseline malaria transmission in a given environment is important to guide malaria control interventions. However, in Uganda, recent information on malaria transmission intensity is lacking. Therefore, a 1-year entomological study was conducted in seven ecologically different sites throughout the country to assess spatial and temporal patterns in malaria transmission intensity. Anopheles gambiae sensu stricto was the main vector in five of the seven study sites, and An. funestus was the most important vector in the two other sites. In a peri-urban village, An. arabiensis contributed substantially to malaria transmission. Clear differences in annual entomological inoculation rates (AEIR) were observed between the study sites, ranging from 4 infective bites per person per year in the southwestern part of the country to >1,500 infective bites per person per year in a swampy area near the Nile River. Between villages with parasite prevalences of >or= 80% in children between 1 and 9 years old, a 4-fold difference in AEIR was observed. Based on the observed behavior of the vectors, insecticide-treated bed nets will be highly effective in controlling malaria. However, in the high transmission areas, additional measures will be needed to reduce the malaria burden to acceptable levels.

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Malaria transmission, infection, and disease at three sites with varied transmission intensity in Uganda: implications for malaria control.

Moses R. Kamya, Emmanuel Arinaitwe, Humphrey Wanzira … (2015)

The intensification of control interventions has led to marked reductions in malaria burden in some settings, but not others. To provide a comprehensive description of malaria epidemiology in Uganda, we conducted surveillance studies over 24 months in 100 houses randomly selected from each of three subcounties: Walukuba (peri-urban), Kihihi (rural), and Nagongera (rural). Annual entomological inoculation rate (aEIR) was estimated from monthly Centers for Disease Control and Prevention (CDC) light trap mosquito collections. Children aged 0.5-10 years were provided long-lasting insecticidal nets (LLINs) and followed for measures of parasite prevalence, anemia and malaria incidence. Estimates of aEIR were 2.8, 32.0, and 310 infectious bites per year, and estimates of parasite prevalence 7.4%, 9.3%, and 28.7% for Walukuba, Kihihi, and Nagongera, respectively. Over the 2-year study, malaria incidence per person-years decreased in Walukuba (0.51 versus 0.31, P = 0.001) and increased in Kihihi (0.97 versus 1.93, P < 0.001) and Nagongera (2.33 versus 3.30, P < 0.001). Of 2,582 episodes of malaria, only 8 (0.3%) met criteria for severe disease. The prevalence of anemia was low and not associated with transmission intensity. In our cohorts, where LLINs and prompt effective treatment were provided, the risk of complicated malaria and anemia was extremely low. However, malaria incidence was high and increased over time at the two rural sites, suggesting improved community-wide coverage of LLIN and additional malaria control interventions are needed in Uganda.

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Function and evolution of a mosquito salivary protein family.

Lene Andersen, J. Mans, Gabriel H. P. M. Ribeiro … (2006)

Saliva of blood-sucking arthropods contains a complex and diverse mixture of antihemostatic, antiinflammatory, and immunomodulatory compounds. The D7 salivary family of proteins is abundantly expressed in blood-feeding Diptera and is distantly related to the odorant-binding protein superfamily. In mosquitoes, two subfamilies exist, the long and short D7 proteins. Ticks and kissing bugs evolved salivary lipocalins that act as efficient scavengers of biogenic amines, and a similar function was postulated for the D7 proteins. Accordingly, we expressed the five members of the small D7 family of the African malaria vector Anopheles gambiae and a D7 long form from Aedes aegypti and showed by isothermal microcalorimetry, a modified and very sensitive non-equilibrium chromatography/spectrum distortion method, and by smooth muscle bioassay that four of these five short D7 proteins and the D7 long form bind serotonin with high affinity, as well as histamine and norepinephrine. The nonbinding D7 protein is poorly expressed in the salivary glands and appears to be on the path to becoming a pseudogene. Scavenging of host amines would antagonize their vasoconstrictor, platelet-aggregating, and pain-inducing properties. It appears that counteracting biogenic amines is of strong adaptive value in the convergent evolution of arthropods to hematophagy. This adaptation has been solved independently in ticks, bugs, and mosquitoes by co-option of either member of the lipocalin or, as shown here, by the odorant-binding protein families.

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Author and article information

Contributors

Brenda Oseno: osenob@gmail.com

Faith Marura: FMarura@kemri-wellcome.org

Rodney Ogwang: ROgwang@kemri-wellcome.org

Martha Muturi: MMuturi@kemri-wellcome.org

James Njunge: JNjunge@kemri-wellcome.org

Irene Nkumama: INailain@kemri-wellcome.org

Robert Mwakesi: RMwakesi@kemri-wellcome.org

Kennedy Mwai: KMwai@kemri-wellcome.org

Martin K. Rono: MRono@kemri-wellcome.org

Ramadhan Mwakubambanya: mwakubaram@gmail.com

Faith Osier: FOsier@kemri-wellcome.org

James Tuju:

ORCID: http://orcid.org/0000-0002-0624-1791

Jtuju@kemri-wellcome.org

Journal

Journal ID (nlm-ta): Parasit Vectors

Journal ID (iso-abbrev): Parasit Vectors

Title: Parasites & Vectors

Publisher: BioMed Central (London )

ISSN (Electronic): 1756-3305

Publication date (Electronic): 8 January 2022

Publication date PMC-release: 8 January 2022

Publication date Collection: 2022

Volume: 15

Electronic Location Identifier: 11

Affiliations

[1 ]KEMRI-Wellcome Trust Research Programme CGMRC, P.O. Box 230-80108, Kilifi, Kenya

[2 ]GRID grid.8301.a, ISNI 0000 0001 0431 4443, Egerton University, ; P.O. Box 536-20115, Nakuru, Kenya

[3 ]GRID grid.449370.d, ISNI 0000 0004 1780 4347, Pwani University, ; P.O. Box 195-80108, Kilifi, Kenya

[4 ]GRID grid.5253.1, ISNI 0000 0001 0328 4908, Heidelberg University Hospital, ; Neuenheimer Feld, 672 69120 Heidelberg, Germany

[5 ]GRID grid.11951.3d, ISNI 0000 0004 1937 1135, School of Public Health, , University of the Witwatersrand, ; 1 Jan Smuts Avenue, Braamfontein 2000, Johannesburg, South Africa

Author information

James Tuju http://orcid.org/0000-0002-0624-1791

Article

Publisher ID: 5130

DOI: 10.1186/s13071-021-05130-5

PMC ID: 8742437

PubMed ID: 34996508

SO-VID: 7ccf86d3-3123-47b4-8533-4eba2811e03e

License:

Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

History

Date received : 15 June 2021

Date accepted : 11 December 2021

Funding

Funded by: FundRef http://dx.doi.org/10.13039/100004440, Wellcome Trust;

Award ID: 107769/Z/10/Z

Award Recipient : Brenda Oseno

Funded by: FundRef http://dx.doi.org/10.13039/501100001713, European and Developing Countries Clinical Trials Partnership;

Award ID: TMA2015SF-1001

Award Recipient : Faith Osier

Custom metadata

ScienceOpen disciplines: Parasitology

Keywords: biomarker of exposure,anopheles gambiae,plasmodium falciparum,infectious bites,malaria

Data availability:

ScienceOpen disciplines: Parasitology

Keywords: biomarker of exposure, anopheles gambiae, plasmodium falciparum, infectious bites, malaria

Characterization of Anopheles gambiae D7 salivary proteins as markers of human–mosquito bite contact

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Abstract

Background

Methods

Results

Conclusions

Graphical abstract

Supplementary Information

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CHAIN Network Collection

Most cited references 30

Variation in malaria transmission intensity in seven sites throughout Uganda.

Malaria transmission, infection, and disease at three sites with varied transmission intensity in Uganda: implications for malaria control.

Function and evolution of a mosquito salivary protein family.

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